Elsevier

Organic Geochemistry

Volume 69, April 2014, Pages 70-75
Organic Geochemistry

Identification of isoprenoid glycosidic glycerol dibiphytanol diethers and indications for their biosynthetic origin

https://doi.org/10.1016/j.orggeochem.2014.02.005Get rights and content

Highlights

  • Novel class of archaeal lipids (1G-GDDs) identified using HPLC-MS.

  • They are likely a product of biosynthesis rather than diagenesis.

  • Archaea may modify the membrane lipids or use unknown lipid biosynthetic pathway.

  • Method for separation of polar and apolar lipids described.

  • Novel acid hydrolysis method for removing lipid head groups reported.

Abstract

A series of archaeal lipid biomarkers, the isoprenoid glycerol dibiphytanol diethers (GDDs), was recently described and proposed to represent either biosynthetic intermediates or diagenetic products of the relatively more abundant glycerol dibiphytanyl glycerol tetraether (GDGT) lipids (Liu, X.-L., Lipp, J.S., Schröder, J.M., Summons, R.E., Hinrichs, K.-U., 2012. Isoprenoid glycerol dialkanol diethers: a series of novel lipids in marine sediments. Organic Geochemistry 43, 50–55). Here we report a novel series of polar lipids comprising a glycosidic head group and GDD core lipids with varying cycloalkyl distributions (1G-GDDs), which were found in estuarine and hot spring sediments, as well as in a pure culture of the mesophilic thaumarchaeon Nitrosopumilus maritimus. 1G-GDDs represented up to 4% of the corresponding monoglycosidic GDGTs (1G-GDGTs). The distinct cycloalkyl distribution patterns of these intact polar lipids (IPLs) and detection of 1G-GDDs in an archaeal culture suggest a biosynthetic source of 1G-GDDs rather than formation exclusively via diagenetic removal of a glycerol moiety from 1G-GDGTs.

Introduction

Recent advances in liquid chromatography and mass spectrometry have promoted the identification and quantification of novel archaeal membrane lipid biomarkers (e.g. Knappy et al., 2009, Yoshinaga et al., 2011, Liu et al., 2012a, Liu et al., 2012b), allowing more comprehensive investigations of archaeal distributions, metabolism and response to environmental conditions. For example, Liu et al., 2012b, Knappy and Keely, 2012 described a novel series of isoprenoid glycerol dialkanol diether lipids (GDDs; Fig. 1) found in marine sediments. They were proposed to comprise a glycerol moiety bound to two biphytanols (free OH on the terminal carbons) via two ether linkages. They therefore differ from the classical glycerol dibiphytanyl glycerol tetraethers (GDGTs; e.g. De Rosa and Gambacorta, 1988), given the lack of two ether linkages to the second terminal glycerol backbone moiety. The proposed GDD core lipids were therefore suggested to represent either degradation products, possibly formed as intermediates during lipid recycling (cf. Takano et al., 2010, Liu et al., 2012b), or biosynthetic intermediates of GDGTs.

GDGT biosynthesis is not fully constrained but several authors have proposed head-to-head condensation of two molecules of glycerol diphytanyl diethers (i.e. archaeol) as a likely mechanism (e.g. Nemoto et al., 2003, Koga and Morii, 2007). Assuming this route of biosynthesis for GDGTs, GDDs would thus represent degradation products of GDGTs after the loss of a glycerol backbone or, as speculated by Liu et al., 2012b, Knappy and Keely, 2012, GDDs may derive from an alternative biosynthetic pathway and could react with an activated glycerol moiety to form two ether bonds and thereby a GDGT core lipid.

We applied the chromatographic method described by Zhu et al. (2013) to investigate intact polar lipid (IPL) and core lipid (CL) distributions in extracts of estuarine and hot spring sediments, as well as a pure archaeal culture (Nitrosopumilus maritimus), a cosmopolitan, mesophilic, ammonia-oxidizing thaumarchaeon (Könneke et al., 2005) grown routinely in our laboratory. This chromatographic separation strategy afforded identification of an intact polar GDD lipid series with one glycosidic head group (1G-GDDs). Assuming that the glycosidic bond of a 1G-GDGT is more susceptible to hydrolysis than the ether bound glycerol (e.g. after mild acid hydrolysis; Liu et al., 2012b), the discovery of a 1G-GDD supports a distinct biological origin of GDD lipids as functional membrane constituents or biosynthetic intermediates.

Section snippets

Sample collection and extraction

Estuarine sediment (ca. 50 cm push core) was collected from the White Oak River (WOR) estuary (34.743°N, 77.124°W) in October 2010, transported to the laboratory and sliced at 2 cm intervals. An aliquot of each interval was wrapped in pre-combusted Al foil and stored at −20 °C until extraction. Hot spring sediment (0–1 cm) was collected from the Great Boiling Spring in the Great Basin, Nevada, USA, as described by Zhang et al. (2013). The ambient temperature and pH were 72.1 °C and 7.1,

1G-GDD identification

1G-GDDs were recognizable after UHPLC-RP-ESI-QTOF-MS from the characteristic staircase elution pattern of biphytanyl ether lipids with 0–5 rings (Zhu et al., 2013), with [M+H]+ at m/z 1408.350, 1406.334, 1404.319, 1402.303, 1400.287 and 1398.272, respectively, which eluted just before the 1G-GDGT series (Fig. 2A and B). The exact masses of the 1G-GDD series, including [M+H]+, [M+NH3]+ and [M+Na]+, were within 5 ppm of expected values. MS2 fragmentation of these ions yielded a loss of 162 Da,

Conclusions

The identification of 1G-GDDs extends the structural diversity of the recently discovered, widespread class of diether glycerolipids and has important implications for the geobiological significance of these compounds. 1G-GDDs were observed with cycloalkyl distributions that were distinct from 1G-GDGTs and GDD-CLs. Based on these observations and the detection of 1G-GDDs and GDD-CLs in an archaeal culture, we conclude that GDD lipids are at least in part a product of biosynthesis, which could

Acknowledgements

The work was primarily funded by European Research Council Advanced Grant 247153 awarded to K.-U.H., C.Z. was funded by the Deutsche Forschungsgemeinschaft (DFG) via a postdoctoral fellowship by the Research Center/Cluster of Excellence MARUM; F.E. and M.K. were supported by the DFG through the Gottfried Wilhelm Leibniz Award to K.-U.H. We are grateful of C. Zhang for providing the hot spring sample. C. Lazar and S. Ghobrial assisted with collection of estuarine sediment and N. Goldenstein and

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